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Molecular Evolution of Antigen-Processing Genes in Salamanders: Do They Coevolve withMHCClass I Genes?

Genome Biology and Evolution, vol. 13

Abstract

Proteins encoded by antigen-processing genes (APGs) prepare antigens for presentation by the major histocompatibility complex class I (MHC I) molecules. Coevolution between APGs and MHC I genes has been proposed as the ancestral gnathostome condition. The hypothesis predicts a single highly expressed MHC I gene and tight linkage between APGs and MHC I. In addition, APGs should evolve under positive selection, a consequence of the adaptive evolution in MHC I. The presence of multiple highly expressed MHC I genes in some teleosts, birds, and urodeles appears incompatible with the coevolution hypothesis. Here, we use urodele amphibians to test two key expectations derived from the coevolution hypothesis: 1) the linkage between APGs and MHC I was studied in Lissotriton newts and 2) the evidence for adaptive evolution in APGs was assessed using 42 urodele species comprising 21 genera from seven families. We demonstrated that five APGs (PSMB8, PSMB9, TAP1, TAP2, and TAPBP) are tightly linked (<0.5 cM) to MHC I. Although all APGs showed some codons under episodic positive selection, we did not find a pervasive signal of positive selection expected under the coevolution hypothesis. Gene duplications, putative gene losses, and divergent allelic lineages detected in some APGs demonstrate considerable evolutionary dynamics of APGs in salamanders. Overall, our results indicate that if coevolution between APGs and MHC I occurred in urodeles, it would be more complex than envisaged in the original formulation of the hypothesis.

Authors 12

  1. Gemma Palomar corresponding

    Jagiellonian University

    Affiliation as printed

    Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland

  2. Jagiellonian University

    Affiliation as printed

    Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland

  3. Leiden University · Naturalis Biodiversity Center

    Affiliation as printed

    Institute of Biology Leiden, Leiden University, The Netherlands

    Naturalis Biodiversity Center, Leiden, The Netherlands

  4. University of Connecticut

    Affiliation as printed

    Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut, USA

  5. Charles University

    Affiliation as printed

    Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic

  6. Naturalis Biodiversity Center

    Affiliation as printed

    Naturalis Biodiversity Center, Leiden, The Netherlands

  7. Centre National de la Recherche Scientifique · University of Milan · Laboratoire d'Écologie Alpine · Université Savoie Mont Blanc · Université Grenoble Alpes

    Affiliation as printed

    Department of Environmental Sciences and Policy, University of Milano, Italy

    Laboratoire d’Ecologie Alpine (LECA), CNRS, Université Grenoble Alpes and Université Savoie Mont Blanc, Grenoble, France

  8. University of the Ryukyus

    Affiliation as printed

    Department of Advanced Genomic and Laboratory Medicine, Graduate School of Medicine, University of the Ryukyus, Nishihara-cho, Japan

  9. Oklahoma State University · Seoul National University

    Affiliation as printed

    Department of Integrative Biology, Oklahoma State University, Stillwater, Oklahoma, USA

    School of Biological Sciences, Seoul National University, South Korea

  10. Charles University

    Affiliation as printed

    Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic

  11. Jagiellonian University

    Affiliation as printed

    Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland

  12. Wiesław Babik corresponding

    Jagiellonian University

    Affiliation as printed

    Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland

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References 90